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Feature Review
Neural mechanisms of motivated forgetting Michael C. Anderson1,2 and Simon Hanslmayr3,4 1
MRC Cognition and Brain Sciences Unit, University of Cambridge, Cambridge, UK Behavioural and Clinical Neuroscience Institute, University of Cambridge, Cambridge, UK 3 School of Psychology, University of Birmingham, Birmingham, UK 4 Department of Psychology – Zukunftskolleg, University of Konstanz, Konstanz, Germany 2
Not all memories are equally welcome in awareness. People limit the time they spend thinking about unpleasant experiences, a process that begins during encoding, but that continues when cues later remind someone of the memory. Here, we review the emerging behavioural and neuroimaging evidence that suppressing awareness of an unwelcome memory, at encoding or retrieval, is achieved by inhibitory control processes mediated by the lateral prefrontal cortex. These mechanisms interact with neural structures that represent experiences in memory, disrupting traces that support retention. Thus, mechanisms engaged to regulate momentary awareness introduce lasting biases in which experiences remain accessible. We argue that theories of forgetting that neglect the motivated control of awareness omit a powerful force shaping the retention of our past. A neglected force that shapes retention Over the past century, memory research has focused on passive factors that make us forget. Forgetting has been proposed to result from the decay of memories over time, the accumulation of similar interfering experiences in memory, and changes in physical context that make it harder to recall the past [1]. This historical emphasis on passive factors fits the common assumption that forgetting is a negative outcome and, thus, any process underlying it must happen involuntarily. Although forgetting is often negative, this emphasis neglects a fundamental feature of human existence: not all experiences are pleasant. When reminded of negative events, we are not well disposed towards them and we deliberately limit their tenure in awareness. This process is familiar to most people; a reminder evokes a brief flash of memory and feeling, abruptly followed by efforts to exclude the unwanted memory from awareness. We do this to preserve our emotional state, to protect our sense of self, and sometimes simply to concentrate on what needs to be done. Therefore, any scientific theory of forgetting must include an account of the considerable motivational forces that shape retention. Here, we review the growing research on neural mechanisms underlying motivated forgetting. The term Corresponding author: Anderson, M.C. ([email protected]). 1364-6613/ ß 2014 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/3.0/). http://dx.doi.org/ 10.1016/j.tics.2014.03.002
‘motivated forgetting’ here refers to increased forgetting arising from active processes that down-prioritise unwanted experiences in service of creating or sustaining an emotional or cognitive state. For example, to sustain positive emotions or concentration, belief in some state of affairs, confidence, or optimism, it may be necessary to reduce accessibility of experiences that undermine those states. Here, we focus on neural evidence for the role of inhibitory control processes in the voluntary interruption of mnemonic processing. A core claim is that these inhibitory control processes, widely studied in psychology and cognitive neuroscience, can be targeted flexibly at different stages of mnemonic processing and at different types of representation to modulate the state of traces in memory. In support of this view, we review evidence that inhibition can be engaged either during memory encoding or retrieval to limit retention of unwanted memories. Stopping encoding may disrupt the consolidation of traces already formed, and also prevent further reflection on the experience that would enhance its longevity. By contrast, stopping retrieval disrupts the automatic progression from cues to an associated memory, the persisting effects of which influence whether the experience remains accessible. Both encoding and retrieval stopping terminate an unfolding mnemonic process so that an experience can be excluded from conscious awareness. Through these efforts to terminate awareness, attentional control interacts with traces in episodic memory to shape what we do and do not remember of our past. Inhibitory control at encoding An effective way of keeping an unwanted memory from being retrieved in the future is to disrupt and truncate its encoding. These processes are investigated with directed forgetting paradigms, in which participants receive a cue to forget information that they just acquired [2]. Hundreds of studies conducted over the past 50 years reveal that humans can readily implement such forgetting instructions, demonstrating that motivation indeed shapes encoding. Inhibition has been proposed to have a role in stopping encoding processes in these procedures, although passive factors also are likely to have a role (e.g., [3]). We focus here on evidence indicating a distinct contribution of inhibitory control in actively limiting the encoding of unwanted experience. This evidence has been collected with the Trends in Cognitive Sciences xx (2014) 1–14
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Feature Review Glossary Accessibility versus availability: : a theoretical distinction on why memory retrieval can fail. We may fail to retrieve memories because we do not access a stored memory (i.e., accessibility) or because the memory is not available anymore in the system (i.e., availability). Brain oscillations: : regular fluctuations visible in the EEG and/or magnetoencephalogram (MEG), most likely reflecting summated excitatory and inhibitory postsynaptic potentials. Brain oscillations occur at different distinct frequencies (up to 150 Hz) and have an important role in synchronising neural assemblies [104] and shaping synaptic plasticity [35]. Cue independence: : the tendency for suppression-induced forgetting to generalise to novel test cues other than the one originally used as a cue during retrieval suppression. Direct suppression: : a method of limiting awareness of an unwanted memory when a reminder appears in which a person disengages the retrieval process to either prevent the memory for coming to mind, or to limit its time in awareness. Inhibition is thought to be a key process in overriding the natural operation of the retrieval mechanism. Effective connectivity analysis: : a form of connectivity analysis that allows one to infer not only that neural activity in two distinct regions is related (statistically), but also the directional nature of that relation. Effective connectivity analyses, such as dynamic causal modelling, permit causal inferences about the influence of one brain region on another in conditions of interest. Episodic context: : the spatiotemporal environment in which a stimulus is encountered. The representation of this context and its association to a stimulus form a fundamental feature of episodic memory of the stimulus. Context can also refer to internal states that get associated to a stimulus (e.g., mood or incidental thoughts), which is sometimes referred to as ‘mental context’. Event-related potential (ERP): : a time-varying brain signal with positive and negative deflections (so-called ‘components’), obtained by averaging over several EEG segments corresponding to a task or stimulus. Fading affect bias: : the documented tendency for negative emotions associated with personal experiences to decline more quickly over time compared with positive emotions. Inhibitory control: : a control process that downregulates activity of interfering or otherwise unwanted representations in the service of a current task or goal, reducing their influence on cognition and behaviour. Late positive component (LPC): : a positive ERP component related to episodic retrieval. During a retrieval task, the LPC emerges approximately 400–800 ms after stimulus onset, is maximal over parietal recording sites, and is assumed to reflect retrieval of contextual details of the study episode (i.e., recollection [105]). Long-range synchrony: : synchronisation between distant cell populations separated by several centimetres (e.g., frontal and parietal). Long-range synchrony is usually estimated based on the co-variation of oscillatory phase between two recording cites. Mnemic neglect: : the tendency for people to have a higher rate of forgetting for negative feedback about themselves and their performance, than for neutral or positive feedback, even when encoding time is matched. N2: : a negative ERP component related to cognitive control, and often associated with motor response inhibition. The N2 refers to enhanced frontocentral negativity typically approximately 150–400 ms. Repetition priming: : improved performance in processing a stimulus arising from prior exposure to the stimulus. Repetition suppression: : the finding that repetitions of a stimulus elicit less neural activity in areas involved in processing the stimulus, compared with nonrepeated stimuli, taken to be a marker of memory for the stimulus. Repetitive transcranial magnetic stimulation (rTMS): : a technique commonly used to stimulate a specific brain area by applying a time-varying magnetic field that induces electric current flow in the brain. Selective rehearsal: : a passive, noninhibitory account used to explain the reduced memory performance for to-be-forgotten items, relative to to-beremembered items. Socially shared retrieval-induced forgetting: : when a person is recounting an experience shared by listeners, the tendency for the listeners to later forget (at a higher rate) details not recounted by the speaker. The higher rate of forgetting is thought to arise from listeners covertly retrieving the experience as it is being recounted and, consequently, inducing retrieval-induced forgetting on nonretrieved knowledge. Suppression-induced forgetting: : in the TNT procedure, impaired recall of nothink items, compared with baseline memories that are neither retrieved nor suppressed. Think/no-think procedure (TNT): : the main procedure used to study retrieval suppression, whereby people are repeatedly prompted with cues to memories and asked to either retrieve (think) the memory, or to stop its retrieval (nothink), with the result that suppressed items are more poorly recalled on later tests. Thought substitution: : a method of preventing retrieval of an unwanted memory when a reminder appears in which a person generates alternative thoughts associated to the reminder to occupy awareness.
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item-method [4] and list-method [5] directed forgetting procedures (Box 1). Item-method directed forgetting Item-method directed forgetting has a long tradition in cognitive psychology [4]. This effect is robust, as reflected by the range of conditions under which it has been reported, including both explicit and implicit memory tests [6,7]. Item-method directed forgetting usually has been explained in terms of selective rehearsal (see Glossary) according to which to-be-forgotten items are spared from further processing and are subject to passive forgetting, whereas to-be-remembered items are actively rehearsed [2]. Interestingly, the occurrence of item-method directed forgetting in recognition tests has been used as an argument for passive, noninhibitory explanations, because some have argued that inhibition should only temporarily reduce the accessibility of the affected items and, therefore, it should be possible to release these items from inhibition later [2]. Although selective rehearsal is a common interpretation of item-method directed forgetting [2], recent behavioural and neural evidence indicates that inhibitory control over episodic encoding may have a bigger role than has been acknowledged. For example, the selective rehearsal account emphasises processes acting on to-be-remembered items, which are rehearsed more extensively and elaborately when the cue to remember is given. Therefore, the system should experience more cognitive load in the remember compared to the ‘forget’ condition, in which people can simply drop the to-be-forgotten item from working memory. This prediction was tested in several experiments in which participants performed a secondary task after the remember and/or forget cue was given [8,9]. However, contrary to the selective rehearsal account, the forget condition was more effortful than the remember condition, as reflected by slower reaction times to perform the secondary task during execution of the forget instruction. Moreover, stopping a motor response after the cue is more successful in the forget compared with the remember condition [9], suggesting that forget cues trigger similar inhibitory mechanisms to those engaged when stopping a motor action [10]. However, further clarification of this possibility is needed [9]. These results clearly imply that an active process contributes to item-method directed forgetting [11], and raise the possibility that it is inhibitory in nature. This possibility is consistent with evidence that directed forgetting cues lead to the removal of items from working memory and not merely to passive decay [12,13]. Several recent functional (f)MRI studies support the hypothesis that item-method directed forgetting engages an active process that inhibits ongoing encoding [14–18]. These studies consistently indicate that attempting to forget a recent item engages prefrontal and parietal regions, suggesting that forgetting is effortful, consistent with behavioural findings [15,16,18]. The right superior and middle frontal gyrus (approximately BA 9/10), and the right inferior parietal lobe (approximately BA 40) are consistently more active during intentional forgetting (to-be-forgotten items that are actually forgotten) compared with incidental forgetting (to-be-remembered items
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Feature Review
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Box 1. Item and list-method directed forgetting In studies of directed forgetting, two procedures are generally used: the item-method and the list-method (see [1]). These paradigms are illustrated in Figure I. As illustrated in Figure IA, in item-method directed forgetting, participants study items one at a time, and each item is followed by a forget (F) or remember (R) instruction. Later, memory for all items is tested. As shown in Figure IB, in list-method directed forgetting, a entire list of items is first studied, followed by a F or R instruction. A second list is then studied, usually followed by a R
(A)
instruction. At the end, a recall test occurs. Figure IC compares the typical behavioural results obtained in item-method (Figure ICi) and list-method (Figure ICii) directed forgetting. Figure ICii shows the twofold effect of the forget cue on the recall test, with forgetting of list-1 items and enhancement of list-2 items. In both paradigms, participants do not know in advance whether they should forget or remember the respective item. Thus, the control processes mediating these effects must act on memory representations and not the initial perception of an event.
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Figure I. The item and list-methods for studying directed forgetting, along with the typical pattern of findings (for real examples, see [8] and [5,25], respectively).
that are forgotten (Figure 1A) [15,16,18]. Although these findings suggest that intentional forgetting recruits additional processes beyond those associated with incidental forgetting, these activations do not specify the nature of those processes. For example, activations during forget trials might reflect engagement of the default mode network, which is characterised by positive blood oxygenation level-dependent (BOLD) correlations between superior prefrontal and parietal cortex during rest [19]. Thus, these
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findings may simply reflect a greater incidence of passive rest during forget trials compared with remember trials. However, speaking against this view, connectivity analyses show that activity in the right dorsolateral prefrontal cortex (DLPFC) during forget trials predicts decreased activity in the left hippocampus, especially during successful intentional forgetting [18]. This latter result is incompatible with the default mode network hypothesis, which predicts the opposite (positive) connectivity pattern
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Figure 1. Neural correlates of directed forgetting (DF). (A) An activation map of a recent item-method directed forgetting functional (f)MRI study [18]. Red areas illustrate significant voxels (P think
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Figure 3. How suppressing retrieval reduces the unconscious influence of unwanted memories, via neocortical inhibition [67]. (A) Adaptation of the think/no-think (TNT) procedure (67). After learning word–object associations, participants either repeatedly retrieved (think) or suppressed (no-think) objects, using direct suppression [88,93]. On the final test, participants viewed objects distorted by noise that were gradually revealed, and participants indicated when they could identify the distorted object. (B) Suppressing retrieval activated the right dorsolateral prefrontal cortex (DLPFC) (i), and reduced activity in fusiform gyrus (ii) (effective connectivity analyses established that the former modulated the latter). (C) Behavioural and neural aftereffects of suppressing visual memories. All objects showed repetition priming (speeded identification time), relative to novel objects, but this was reduced for suppressed objects (i). Similarly, all studied objects showed neural priming (reduced neural activity) in fusiform gyrus and the lateral occipital complex, relative to novel objects, but this was partially reversed for suppressed objects (ii). Negative coupling between DLPFC and fusiform gyrus predicted the magnitude of the reversal in neural priming on the final perceptual identification test (iii). Abbreviations: DCM, Dynamic Causal Modelling; MGF, middle frontal gyrus; ROI, region of interest.
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Feature Review control. Importantly, reductions in neural priming were well predicted by inhibitory control during the earlier TNT phase: effective connectivity analyses showed that suppressing retrieval led to negative coupling between right DLPFC and fusiform gyrus, the magnitude of which predicted the reduced neural priming in fusiform cortex on the later perception test. Thus, suppressing awareness of visual memories reduced activity not only in the hippocampus, but also in visual cortex, limiting momentary visual consciousness of the objects and disrupting later perceptual memory. This finding complements fMRI and behavioural evidence for mechanisms that purge unwanted contents from visual working memory, illustrating their inhibitory aftereffects on visual neocortex [12,103]. In the foregoing study, inhibitory control may target visual object regions to reduce reactivation arising from intrusive memories, reactivation that may arise through recurrent connections from the hippocampus [67]. This possibility suggests a broad principle of memory control: when reminders evoke activity in content-specific areas, those areas will be targeted by control [67], affecting content in those regions. Suppressing emotional memories may provide a second example. When a memory elicits a strong emotional response, regions involved in affect may be suppressed. Consistent with this, suppressing aversive scenes (e.g., violence and death) reduces activity in both the hippocampus and the amygdala ([63,64] although see [89]). Reducing activity in the amygdala could disrupt emotional learning associated with the event, much like hippocampal
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or fusiform modulation disrupts episodic memory or object priming, respectively. Such modulation may contribute to the widely observed fading affect bias in autobiographical memory (Box 4). However, because it remains unknown whether DLPFC is effectively connected with the amygdala during suppression, reduced activity may instead be a passive side effect of downregulating recollective activity in the hippocampus, and the resulting exclusion of the unpleasant memory from awareness. However, even given this possibility, reduced amygdala activity may reflect success at achieving a central goal of motivated forgetting in many real-life circumstances: reduced negative affect arising from the successful voluntary control of mnemonic awareness. However, the paradigms discussed here differ from reallife circumstances in important ways. No directed forgetting or retrieval suppression paradigm, for example, captures the natural motivations that people have for suppressing awareness of memories that they find personally unwelcome (Box 4). Although the neural mechanisms identified here likely implement motivated forgetting ‘in the wild’, this work may underestimate the impact on retention for someone with a true sustained motive. Understanding the effects of personal motivation will likely entail a step away from controlled materials, towards autobiographical experiences unique to an individual. However, for now, the fundamental control processes that limit mnemonic processing are emerging, and will inform our view of how people wilfully shape retention of their personal experiences.
Box 4. Motives for motivated forgetting Below is a sampling of motives that may trigger motivated forgetting, illustrating the breadth of contexts in which these neural mechanisms are likely to operate. Regulating negative affect Memories that evoke fear, anger, sadness, guilt, shame, anxiety, and embarrassment trigger people to regulate their emotions by suppressing offending memories [118]. In the short term, emotion regulation helps to reduce negative feelings, returning to a state of homeostasis [119]. In the long term, this may contribute to the reliably reduced frequency of negative autobiographical memories compared with positive ones for most people [120,121]. It may also contribute to the fading affect bias, wherein affect associated with negative memories fades more rapidly than other affective content [120,122]. Justifying inappropriate behaviour People sometimes engage in dishonest acts that conflict with their desire to be moral. This dissonance creates discomfort that people may reduce via motivated forgetting. In experimental settings, people show increased forgetting of moral rules after behaving dishonestly (e.g., cheating) even though they are equally likely to remember morally irrelevant rules as participants who do not cheat [123,124]. Maintaining beliefs and attitudes People’s beliefs are often resistant to contradictory evidence. This resilience may be supported by selectively forgetting information not congenial to one’s beliefs. For example, republicans and democrats show enhanced directed forgetting for attitude statements that are incongruent with their beliefs, compared with congruent statements [125]. Moreover, one’s memory can be shaped by selectively recounting elements of an event [126–128], a form of thought substitution [88,129]. Intriguingly, this can undermine listeners’ memories of the omitted facts, a phenomenon called ‘socially shared retrieval-induced forgetting’ [126–128].
Deceiving others and oneself Memory inhibition may contribute to creating a state of false belief, necessary to deceive others and even oneself [130]. Consistent with this, people can use retrieval suppression to disguise guilty knowledge of a crime when confronting reminders to the crime event, effectively eliminating EEG markers of recollection [131]. Preserving self image People protect their self-image by selectively remembering feedback consistent with positive traits and forgetting that which threatens their sense of self. This robust ‘mnemic neglect’ effect arises despite holding encoding time constant, and is only present for encoding traits in relation to oneself, not others. Mnemic neglect is markedly attenuated, if, before encoding, people receive positive, self-enhancing feedback on a separate task, reducing their urge for selfprotection [132–134]. Forgiving others Interpersonal relations are sometimes accompanied by the need to forgive relationship partners for offenses that provoke anger. Individual differences in forgiveness are well predicted by inhibitory control ability [135], and it has been argued that memory inhibition may be key in overcoming rumination about transgressions [136]. Forgiving and forgetting may indeed be closely related. Maintaining attachment The need to maintain an attachment relationship with a parent, guardian, or powerful authority figure (e.g., a boss) may be essential to survive or thrive in an environment. Behaviours that promote good relations or attachment to the influential individual may motivate selective remembering of experiences compatible with attachment [129], and forgetting of those that are incompatible. Betrayal trauma theory, for example, posits that motivated forgetting of childhood abuse by a trusted caretaker is driven by this attachment need [137,138]. 11
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Feature Review Concluding remarks In this article, we reviewed evidence for the active role that people have in shaping retention. We focussed in particular on the function of inhibitory control processes in modulating the efficacy of memory processes at both encoding and retrieval. If, upon encoding an experience, people intentionally exclude the event from awareness, retention of the experience is impaired, compared with cases in which they intend to remember the event. Although this deficit arises from several sources, one factor is the termination of encoding by inhibition, and the disruption of episodic traces formed up until that point. Similarly, upon encountering reminders to existing memories, people can engage inhibitory control to stop retrieval. In both encoding and retrieval suppression, multiple sources of evidence indicate that control mechanisms mediated by the prefrontal cortex interrupt mnemonic function and impair memory. Thus, excluding unwanted memories from awareness does not merely deprive experiences of further rehearsal, it contributes to forgetting by disrupting the suppressed memory. However, much remains to be understood about the pathways and neural mechanisms of this suppression (Box 5). Understanding forgetting is one of the fundamental goals of the science of memory. We have argued that the focus on incidental forgetting mechanisms over the past century, although profitable, has profoundly neglected one of the most systemic forces shaping retention of life events: ourselves. Forgetting does indeed happen due to forces beyond our control; but we are, without a doubt, conspirators in our own forgetting. We wield control over mnemonic processes, choosing, among life’s experiences, winners and losers for the potent effects of attention, reflection, and suppression. Modern behavioural and neurobiological research is revealing how our momentary choices to stop encoding or retrieval unfold in the brain, and how control processes disrupt the normal functioning of memory. These momentary choices are, in turn, driven by our affective, motivational, social, and cognitive goals. Thus, to understand why human beings remember what they do of their life histories, a scientific theory of forgetting must account for the foundational control mechanisms that implement the ongoing and active role that we play in shaping the fate of experience in memory. Box 5. Outstanding questions How do motivation and emotion influence the ability to inhibit memories? What are the critical pathways by which DLPFC modulates neural activity in the hippocampus or neocortex to suppress memories? Is there plasticity in the networks underlying memory control that might be exploited to train people’s management of intrusive memories? What neural changes underlie the disrupted memory performance associated with memory inhibition and is it related to reconsolidation? Are the inhibitory control mechanisms that support the stopping of encoding and retrieval the same? How is activity in the prefrontal–hippocampal memory control network orchestrated by means of brain oscillations? Do cases of psychogenic amnesia arise from motivated forgetting mechanisms discussed here, or is psychogenic amnesia qualitatively different? 12
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Acknowledgements This work was supported by a grant from the UK Medical Research Council (MC-A060-5PR00) to M.C.A. and by a grant from the Deutsche Forschungsgemeinschaft (HA 5622/1-1) to S.H. The authors thank Roland Benoit, Pierre Gagnepain, and Avery Rizio for assistance in creating Figures 1, 2, and 3, and Jonathan Fawcett for providing comments on the manuscript.
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Feature Review
Neural mechanisms of motivated forgetting Michael C. Anderson1,2 and Simon Hanslmayr3,4 1
MRC Cognition and Brain Sciences Unit, University of Cambridge, Cambridge, UK Behavioural and Clinical Neuroscience Institute, University of Cambridge, Cambridge, UK 3 School of Psychology, University of Birmingham, Birmingham, UK 4 Department of Psychology – Zukunftskolleg, University of Konstanz, Konstanz, Germany 2
Not all memories are equally welcome in awareness. People limit the time they spend thinking about unpleasant experiences, a process that begins during encoding, but that continues when cues later remind someone of the memory. Here, we review the emerging behavioural and neuroimaging evidence that suppressing awareness of an unwelcome memory, at encoding or retrieval, is achieved by inhibitory control processes mediated by the lateral prefrontal cortex. These mechanisms interact with neural structures that represent experiences in memory, disrupting traces that support retention. Thus, mechanisms engaged to regulate momentary awareness introduce lasting biases in which experiences remain accessible. We argue that theories of forgetting that neglect the motivated control of awareness omit a powerful force shaping the retention of our past. A neglected force that shapes retention Over the past century, memory research has focused on passive factors that make us forget. Forgetting has been proposed to result from the decay of memories over time, the accumulation of similar interfering experiences in memory, and changes in physical context that make it harder to recall the past [1]. This historical emphasis on passive factors fits the common assumption that forgetting is a negative outcome and, thus, any process underlying it must happen involuntarily. Although forgetting is often negative, this emphasis neglects a fundamental feature of human existence: not all experiences are pleasant. When reminded of negative events, we are not well disposed towards them and we deliberately limit their tenure in awareness. This process is familiar to most people; a reminder evokes a brief flash of memory and feeling, abruptly followed by efforts to exclude the unwanted memory from awareness. We do this to preserve our emotional state, to protect our sense of self, and sometimes simply to concentrate on what needs to be done. Therefore, any scientific theory of forgetting must include an account of the considerable motivational forces that shape retention. Here, we review the growing research on neural mechanisms underlying motivated forgetting. The term Corresponding author: Anderson, M.C. ([email protected]). 1364-6613/ ß 2014 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/3.0/). http://dx.doi.org/ 10.1016/j.tics.2014.03.002
‘motivated forgetting’ here refers to increased forgetting arising from active processes that down-prioritise unwanted experiences in service of creating or sustaining an emotional or cognitive state. For example, to sustain positive emotions or concentration, belief in some state of affairs, confidence, or optimism, it may be necessary to reduce accessibility of experiences that undermine those states. Here, we focus on neural evidence for the role of inhibitory control processes in the voluntary interruption of mnemonic processing. A core claim is that these inhibitory control processes, widely studied in psychology and cognitive neuroscience, can be targeted flexibly at different stages of mnemonic processing and at different types of representation to modulate the state of traces in memory. In support of this view, we review evidence that inhibition can be engaged either during memory encoding or retrieval to limit retention of unwanted memories. Stopping encoding may disrupt the consolidation of traces already formed, and also prevent further reflection on the experience that would enhance its longevity. By contrast, stopping retrieval disrupts the automatic progression from cues to an associated memory, the persisting effects of which influence whether the experience remains accessible. Both encoding and retrieval stopping terminate an unfolding mnemonic process so that an experience can be excluded from conscious awareness. Through these efforts to terminate awareness, attentional control interacts with traces in episodic memory to shape what we do and do not remember of our past. Inhibitory control at encoding An effective way of keeping an unwanted memory from being retrieved in the future is to disrupt and truncate its encoding. These processes are investigated with directed forgetting paradigms, in which participants receive a cue to forget information that they just acquired [2]. Hundreds of studies conducted over the past 50 years reveal that humans can readily implement such forgetting instructions, demonstrating that motivation indeed shapes encoding. Inhibition has been proposed to have a role in stopping encoding processes in these procedures, although passive factors also are likely to have a role (e.g., [3]). We focus here on evidence indicating a distinct contribution of inhibitory control in actively limiting the encoding of unwanted experience. This evidence has been collected with the Trends in Cognitive Sciences xx (2014) 1–14
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Feature Review Glossary Accessibility versus availability: : a theoretical distinction on why memory retrieval can fail. We may fail to retrieve memories because we do not access a stored memory (i.e., accessibility) or because the memory is not available anymore in the system (i.e., availability). Brain oscillations: : regular fluctuations visible in the EEG and/or magnetoencephalogram (MEG), most likely reflecting summated excitatory and inhibitory postsynaptic potentials. Brain oscillations occur at different distinct frequencies (up to 150 Hz) and have an important role in synchronising neural assemblies [104] and shaping synaptic plasticity [35]. Cue independence: : the tendency for suppression-induced forgetting to generalise to novel test cues other than the one originally used as a cue during retrieval suppression. Direct suppression: : a method of limiting awareness of an unwanted memory when a reminder appears in which a person disengages the retrieval process to either prevent the memory for coming to mind, or to limit its time in awareness. Inhibition is thought to be a key process in overriding the natural operation of the retrieval mechanism. Effective connectivity analysis: : a form of connectivity analysis that allows one to infer not only that neural activity in two distinct regions is related (statistically), but also the directional nature of that relation. Effective connectivity analyses, such as dynamic causal modelling, permit causal inferences about the influence of one brain region on another in conditions of interest. Episodic context: : the spatiotemporal environment in which a stimulus is encountered. The representation of this context and its association to a stimulus form a fundamental feature of episodic memory of the stimulus. Context can also refer to internal states that get associated to a stimulus (e.g., mood or incidental thoughts), which is sometimes referred to as ‘mental context’. Event-related potential (ERP): : a time-varying brain signal with positive and negative deflections (so-called ‘components’), obtained by averaging over several EEG segments corresponding to a task or stimulus. Fading affect bias: : the documented tendency for negative emotions associated with personal experiences to decline more quickly over time compared with positive emotions. Inhibitory control: : a control process that downregulates activity of interfering or otherwise unwanted representations in the service of a current task or goal, reducing their influence on cognition and behaviour. Late positive component (LPC): : a positive ERP component related to episodic retrieval. During a retrieval task, the LPC emerges approximately 400–800 ms after stimulus onset, is maximal over parietal recording sites, and is assumed to reflect retrieval of contextual details of the study episode (i.e., recollection [105]). Long-range synchrony: : synchronisation between distant cell populations separated by several centimetres (e.g., frontal and parietal). Long-range synchrony is usually estimated based on the co-variation of oscillatory phase between two recording cites. Mnemic neglect: : the tendency for people to have a higher rate of forgetting for negative feedback about themselves and their performance, than for neutral or positive feedback, even when encoding time is matched. N2: : a negative ERP component related to cognitive control, and often associated with motor response inhibition. The N2 refers to enhanced frontocentral negativity typically approximately 150–400 ms. Repetition priming: : improved performance in processing a stimulus arising from prior exposure to the stimulus. Repetition suppression: : the finding that repetitions of a stimulus elicit less neural activity in areas involved in processing the stimulus, compared with nonrepeated stimuli, taken to be a marker of memory for the stimulus. Repetitive transcranial magnetic stimulation (rTMS): : a technique commonly used to stimulate a specific brain area by applying a time-varying magnetic field that induces electric current flow in the brain. Selective rehearsal: : a passive, noninhibitory account used to explain the reduced memory performance for to-be-forgotten items, relative to to-beremembered items. Socially shared retrieval-induced forgetting: : when a person is recounting an experience shared by listeners, the tendency for the listeners to later forget (at a higher rate) details not recounted by the speaker. The higher rate of forgetting is thought to arise from listeners covertly retrieving the experience as it is being recounted and, consequently, inducing retrieval-induced forgetting on nonretrieved knowledge. Suppression-induced forgetting: : in the TNT procedure, impaired recall of nothink items, compared with baseline memories that are neither retrieved nor suppressed. Think/no-think procedure (TNT): : the main procedure used to study retrieval suppression, whereby people are repeatedly prompted with cues to memories and asked to either retrieve (think) the memory, or to stop its retrieval (nothink), with the result that suppressed items are more poorly recalled on later tests. Thought substitution: : a method of preventing retrieval of an unwanted memory when a reminder appears in which a person generates alternative thoughts associated to the reminder to occupy awareness.
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item-method [4] and list-method [5] directed forgetting procedures (Box 1). Item-method directed forgetting Item-method directed forgetting has a long tradition in cognitive psychology [4]. This effect is robust, as reflected by the range of conditions under which it has been reported, including both explicit and implicit memory tests [6,7]. Item-method directed forgetting usually has been explained in terms of selective rehearsal (see Glossary) according to which to-be-forgotten items are spared from further processing and are subject to passive forgetting, whereas to-be-remembered items are actively rehearsed [2]. Interestingly, the occurrence of item-method directed forgetting in recognition tests has been used as an argument for passive, noninhibitory explanations, because some have argued that inhibition should only temporarily reduce the accessibility of the affected items and, therefore, it should be possible to release these items from inhibition later [2]. Although selective rehearsal is a common interpretation of item-method directed forgetting [2], recent behavioural and neural evidence indicates that inhibitory control over episodic encoding may have a bigger role than has been acknowledged. For example, the selective rehearsal account emphasises processes acting on to-be-remembered items, which are rehearsed more extensively and elaborately when the cue to remember is given. Therefore, the system should experience more cognitive load in the remember compared to the ‘forget’ condition, in which people can simply drop the to-be-forgotten item from working memory. This prediction was tested in several experiments in which participants performed a secondary task after the remember and/or forget cue was given [8,9]. However, contrary to the selective rehearsal account, the forget condition was more effortful than the remember condition, as reflected by slower reaction times to perform the secondary task during execution of the forget instruction. Moreover, stopping a motor response after the cue is more successful in the forget compared with the remember condition [9], suggesting that forget cues trigger similar inhibitory mechanisms to those engaged when stopping a motor action [10]. However, further clarification of this possibility is needed [9]. These results clearly imply that an active process contributes to item-method directed forgetting [11], and raise the possibility that it is inhibitory in nature. This possibility is consistent with evidence that directed forgetting cues lead to the removal of items from working memory and not merely to passive decay [12,13]. Several recent functional (f)MRI studies support the hypothesis that item-method directed forgetting engages an active process that inhibits ongoing encoding [14–18]. These studies consistently indicate that attempting to forget a recent item engages prefrontal and parietal regions, suggesting that forgetting is effortful, consistent with behavioural findings [15,16,18]. The right superior and middle frontal gyrus (approximately BA 9/10), and the right inferior parietal lobe (approximately BA 40) are consistently more active during intentional forgetting (to-be-forgotten items that are actually forgotten) compared with incidental forgetting (to-be-remembered items
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Feature Review
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Box 1. Item and list-method directed forgetting In studies of directed forgetting, two procedures are generally used: the item-method and the list-method (see [1]). These paradigms are illustrated in Figure I. As illustrated in Figure IA, in item-method directed forgetting, participants study items one at a time, and each item is followed by a forget (F) or remember (R) instruction. Later, memory for all items is tested. As shown in Figure IB, in list-method directed forgetting, a entire list of items is first studied, followed by a F or R instruction. A second list is then studied, usually followed by a R
(A)
instruction. At the end, a recall test occurs. Figure IC compares the typical behavioural results obtained in item-method (Figure ICi) and list-method (Figure ICii) directed forgetting. Figure ICii shows the twofold effect of the forget cue on the recall test, with forgetting of list-1 items and enhancement of list-2 items. In both paradigms, participants do not know in advance whether they should forget or remember the respective item. Thus, the control processes mediating these effects must act on memory representations and not the initial perception of an event.
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Figure I. The item and list-methods for studying directed forgetting, along with the typical pattern of findings (for real examples, see [8] and [5,25], respectively).
that are forgotten (Figure 1A) [15,16,18]. Although these findings suggest that intentional forgetting recruits additional processes beyond those associated with incidental forgetting, these activations do not specify the nature of those processes. For example, activations during forget trials might reflect engagement of the default mode network, which is characterised by positive blood oxygenation level-dependent (BOLD) correlations between superior prefrontal and parietal cortex during rest [19]. Thus, these
(A)
(B)
findings may simply reflect a greater incidence of passive rest during forget trials compared with remember trials. However, speaking against this view, connectivity analyses show that activity in the right dorsolateral prefrontal cortex (DLPFC) during forget trials predicts decreased activity in the left hippocampus, especially during successful intentional forgetting [18]. This latter result is incompatible with the default mode network hypothesis, which predicts the opposite (positive) connectivity pattern
fMRI
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Figure 1. Neural correlates of directed forgetting (DF). (A) An activation map of a recent item-method directed forgetting functional (f)MRI study [18]. Red areas illustrate significant voxels (P think
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Figure 3. How suppressing retrieval reduces the unconscious influence of unwanted memories, via neocortical inhibition [67]. (A) Adaptation of the think/no-think (TNT) procedure (67). After learning word–object associations, participants either repeatedly retrieved (think) or suppressed (no-think) objects, using direct suppression [88,93]. On the final test, participants viewed objects distorted by noise that were gradually revealed, and participants indicated when they could identify the distorted object. (B) Suppressing retrieval activated the right dorsolateral prefrontal cortex (DLPFC) (i), and reduced activity in fusiform gyrus (ii) (effective connectivity analyses established that the former modulated the latter). (C) Behavioural and neural aftereffects of suppressing visual memories. All objects showed repetition priming (speeded identification time), relative to novel objects, but this was reduced for suppressed objects (i). Similarly, all studied objects showed neural priming (reduced neural activity) in fusiform gyrus and the lateral occipital complex, relative to novel objects, but this was partially reversed for suppressed objects (ii). Negative coupling between DLPFC and fusiform gyrus predicted the magnitude of the reversal in neural priming on the final perceptual identification test (iii). Abbreviations: DCM, Dynamic Causal Modelling; MGF, middle frontal gyrus; ROI, region of interest.
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Feature Review control. Importantly, reductions in neural priming were well predicted by inhibitory control during the earlier TNT phase: effective connectivity analyses showed that suppressing retrieval led to negative coupling between right DLPFC and fusiform gyrus, the magnitude of which predicted the reduced neural priming in fusiform cortex on the later perception test. Thus, suppressing awareness of visual memories reduced activity not only in the hippocampus, but also in visual cortex, limiting momentary visual consciousness of the objects and disrupting later perceptual memory. This finding complements fMRI and behavioural evidence for mechanisms that purge unwanted contents from visual working memory, illustrating their inhibitory aftereffects on visual neocortex [12,103]. In the foregoing study, inhibitory control may target visual object regions to reduce reactivation arising from intrusive memories, reactivation that may arise through recurrent connections from the hippocampus [67]. This possibility suggests a broad principle of memory control: when reminders evoke activity in content-specific areas, those areas will be targeted by control [67], affecting content in those regions. Suppressing emotional memories may provide a second example. When a memory elicits a strong emotional response, regions involved in affect may be suppressed. Consistent with this, suppressing aversive scenes (e.g., violence and death) reduces activity in both the hippocampus and the amygdala ([63,64] although see [89]). Reducing activity in the amygdala could disrupt emotional learning associated with the event, much like hippocampal
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or fusiform modulation disrupts episodic memory or object priming, respectively. Such modulation may contribute to the widely observed fading affect bias in autobiographical memory (Box 4). However, because it remains unknown whether DLPFC is effectively connected with the amygdala during suppression, reduced activity may instead be a passive side effect of downregulating recollective activity in the hippocampus, and the resulting exclusion of the unpleasant memory from awareness. However, even given this possibility, reduced amygdala activity may reflect success at achieving a central goal of motivated forgetting in many real-life circumstances: reduced negative affect arising from the successful voluntary control of mnemonic awareness. However, the paradigms discussed here differ from reallife circumstances in important ways. No directed forgetting or retrieval suppression paradigm, for example, captures the natural motivations that people have for suppressing awareness of memories that they find personally unwelcome (Box 4). Although the neural mechanisms identified here likely implement motivated forgetting ‘in the wild’, this work may underestimate the impact on retention for someone with a true sustained motive. Understanding the effects of personal motivation will likely entail a step away from controlled materials, towards autobiographical experiences unique to an individual. However, for now, the fundamental control processes that limit mnemonic processing are emerging, and will inform our view of how people wilfully shape retention of their personal experiences.
Box 4. Motives for motivated forgetting Below is a sampling of motives that may trigger motivated forgetting, illustrating the breadth of contexts in which these neural mechanisms are likely to operate. Regulating negative affect Memories that evoke fear, anger, sadness, guilt, shame, anxiety, and embarrassment trigger people to regulate their emotions by suppressing offending memories [118]. In the short term, emotion regulation helps to reduce negative feelings, returning to a state of homeostasis [119]. In the long term, this may contribute to the reliably reduced frequency of negative autobiographical memories compared with positive ones for most people [120,121]. It may also contribute to the fading affect bias, wherein affect associated with negative memories fades more rapidly than other affective content [120,122]. Justifying inappropriate behaviour People sometimes engage in dishonest acts that conflict with their desire to be moral. This dissonance creates discomfort that people may reduce via motivated forgetting. In experimental settings, people show increased forgetting of moral rules after behaving dishonestly (e.g., cheating) even though they are equally likely to remember morally irrelevant rules as participants who do not cheat [123,124]. Maintaining beliefs and attitudes People’s beliefs are often resistant to contradictory evidence. This resilience may be supported by selectively forgetting information not congenial to one’s beliefs. For example, republicans and democrats show enhanced directed forgetting for attitude statements that are incongruent with their beliefs, compared with congruent statements [125]. Moreover, one’s memory can be shaped by selectively recounting elements of an event [126–128], a form of thought substitution [88,129]. Intriguingly, this can undermine listeners’ memories of the omitted facts, a phenomenon called ‘socially shared retrieval-induced forgetting’ [126–128].
Deceiving others and oneself Memory inhibition may contribute to creating a state of false belief, necessary to deceive others and even oneself [130]. Consistent with this, people can use retrieval suppression to disguise guilty knowledge of a crime when confronting reminders to the crime event, effectively eliminating EEG markers of recollection [131]. Preserving self image People protect their self-image by selectively remembering feedback consistent with positive traits and forgetting that which threatens their sense of self. This robust ‘mnemic neglect’ effect arises despite holding encoding time constant, and is only present for encoding traits in relation to oneself, not others. Mnemic neglect is markedly attenuated, if, before encoding, people receive positive, self-enhancing feedback on a separate task, reducing their urge for selfprotection [132–134]. Forgiving others Interpersonal relations are sometimes accompanied by the need to forgive relationship partners for offenses that provoke anger. Individual differences in forgiveness are well predicted by inhibitory control ability [135], and it has been argued that memory inhibition may be key in overcoming rumination about transgressions [136]. Forgiving and forgetting may indeed be closely related. Maintaining attachment The need to maintain an attachment relationship with a parent, guardian, or powerful authority figure (e.g., a boss) may be essential to survive or thrive in an environment. Behaviours that promote good relations or attachment to the influential individual may motivate selective remembering of experiences compatible with attachment [129], and forgetting of those that are incompatible. Betrayal trauma theory, for example, posits that motivated forgetting of childhood abuse by a trusted caretaker is driven by this attachment need [137,138]. 11
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Feature Review Concluding remarks In this article, we reviewed evidence for the active role that people have in shaping retention. We focussed in particular on the function of inhibitory control processes in modulating the efficacy of memory processes at both encoding and retrieval. If, upon encoding an experience, people intentionally exclude the event from awareness, retention of the experience is impaired, compared with cases in which they intend to remember the event. Although this deficit arises from several sources, one factor is the termination of encoding by inhibition, and the disruption of episodic traces formed up until that point. Similarly, upon encountering reminders to existing memories, people can engage inhibitory control to stop retrieval. In both encoding and retrieval suppression, multiple sources of evidence indicate that control mechanisms mediated by the prefrontal cortex interrupt mnemonic function and impair memory. Thus, excluding unwanted memories from awareness does not merely deprive experiences of further rehearsal, it contributes to forgetting by disrupting the suppressed memory. However, much remains to be understood about the pathways and neural mechanisms of this suppression (Box 5). Understanding forgetting is one of the fundamental goals of the science of memory. We have argued that the focus on incidental forgetting mechanisms over the past century, although profitable, has profoundly neglected one of the most systemic forces shaping retention of life events: ourselves. Forgetting does indeed happen due to forces beyond our control; but we are, without a doubt, conspirators in our own forgetting. We wield control over mnemonic processes, choosing, among life’s experiences, winners and losers for the potent effects of attention, reflection, and suppression. Modern behavioural and neurobiological research is revealing how our momentary choices to stop encoding or retrieval unfold in the brain, and how control processes disrupt the normal functioning of memory. These momentary choices are, in turn, driven by our affective, motivational, social, and cognitive goals. Thus, to understand why human beings remember what they do of their life histories, a scientific theory of forgetting must account for the foundational control mechanisms that implement the ongoing and active role that we play in shaping the fate of experience in memory. Box 5. Outstanding questions How do motivation and emotion influence the ability to inhibit memories? What are the critical pathways by which DLPFC modulates neural activity in the hippocampus or neocortex to suppress memories? Is there plasticity in the networks underlying memory control that might be exploited to train people’s management of intrusive memories? What neural changes underlie the disrupted memory performance associated with memory inhibition and is it related to reconsolidation? Are the inhibitory control mechanisms that support the stopping of encoding and retrieval the same? How is activity in the prefrontal–hippocampal memory control network orchestrated by means of brain oscillations? Do cases of psychogenic amnesia arise from motivated forgetting mechanisms discussed here, or is psychogenic amnesia qualitatively different? 12
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Acknowledgements This work was supported by a grant from the UK Medical Research Council (MC-A060-5PR00) to M.C.A. and by a grant from the Deutsche Forschungsgemeinschaft (HA 5622/1-1) to S.H. The authors thank Roland Benoit, Pierre Gagnepain, and Avery Rizio for assistance in creating Figures 1, 2, and 3, and Jonathan Fawcett for providing comments on the manuscript.
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